The barnacles passively filter food, using tentacle-like cirri, as the host swims through the water. The arrangement is generally considered commensal as it is done at no cost or benefit to the host. However, some whales may make use of the barnacles as protective armor or for inflicting more damage while fighting, which would make the relationship mutualistic where both parties benefit; alternatively, some species may just increase the drag that the host experiences while swimming, making the barnacles parasites.

After hatching, whale barnacles go through six molting stages before searching for a host, being guided to settle by a chemical cue from the host skin. The barnacle creates a crown-shaped shell, and in most instances, deeply embeds itself into the skin for stability while riding a fast-moving host. The shell plates are made of calcium carbonate and chitin.

Whale barnacles may live for up to a year, and often slough off along migration routes or at whale calving grounds. Because of this, fossil whale barnacles can be used to study ancient whale distribution.

Contents

Whale barnacles may have originated from the turtle barnacles (Chelonibiidae)—which attach to turtles, sirenians, and crabs—as a group that changed its specialization to baleen whales.[3] Turtle barnacles are known from before the Early Tertiary which ended 23 million years ago (mya), and whale barnacles probably diverged in the Late Pliocene 3.5 to 3 mya. Chelonibia testudinaria turtle barnacle remains from the Pliocene of Italy seemed to have been associated with right whales (Balaena spp.), and could represent a transitional phase; the lack of competing barnacle species and the softer skin compared to the turtle carapace may have led to a divergence and a dispersal. Since whale barnacles are monophyletic (the family contains a common ancestor and all its descendants), this dispersal only successfully occurred once.[4] Since whale barnacles may become detached from their hosts along migration routes and at breeding grounds, their remains on the seabed are used as indicators of ancient whale distribution and migratory habits, similar to the function of trace fossils.[3][5][6]

In 1916, biologist Henry Augustus Pilsbry differentiated turtle barnacles from whale barnacles and assigned them to Chelonibiinae and Coronulinae, respectively; he also recognized two forms of Coronulinae, coronulid and platylepadi, based on anatomical differences and host preferences. In 1976, the family Coronulidae was redefined to include Coronulinae, Platylepadinae, Chelonibiinae, and Emersoniinae; Coronuloidea was rearranged to include Coronulidae, Tatraclitidae, and Bathylasmatida. In 1981, Coronulidae was reorganized to include the subfamilies Coronulinae, Chelonibiinae, and Xenobalaninae.[5] In 2007, these were redefined as Coronuloidea comprising three families: Coronulidae, Chelonibiidae, and Platylepadidae.[10]

All acorn barnacles create a crown-shaped shell with six to eight plates and a hole at the peak. C. diadema is typically barrel-shaped, has most of the shell emergent from the skin, and has been measured in the North Pacific to reach 39–50 millimetres (1.5–2.0 in) in height. Coronula reginae, which is typically 13–19 millimetres (0.51–0.75 in) high; Cetopirus, which has been recorded in two individuals as 12 and 28 millimetres (0.47 and 1.10 in) high and 53 and 74 millimetres (2.1 and 2.9 in) in diameter, respectively; and Cryptolepas are flattened and deeply embedded in the skin.[14]Tubicinella is tall and tube-shaped with ridges that may serve to prevent the skin from rejecting the barnacle, and typically exceeds 50 millimetres (2.0 in) in height.[10]Xenobalanus has a star-shaped shell deeply embedded into the skin, and develops a long stalk, much like goose barnacles, which hangs off the host;[15][16]Xenobalanus may be around 30 millimetres (1.2 in) in size.[17]

The fleshy appendage exiting the hole—the "apertural shroud"—is more prominently displayed than in other barnacles.[10] The cirri, feeding tentacles which extend out of the aperture, are short and thick, probably enabling them to remain more stable while riding a fast-moving host. Whale barnacles have reduced opercular plates which only partially close the hole at the top, probably because these barnacles lack predators and thus any need to defend themselves.[5] The plates, like in turtle barnacles, are made of calcium carbonate and chitin.[10] Inside the plates, the soft barnacle itself is encased in a cuticle which is periodically molted.[18] When they are shed from the host, whale barnacles can leave round marks,[14] but Xenobalanus leaves a unique star-shaped scar.[3]C. diadema, based on infestation sizes and the number of juveniles that are present as the year progresses, may have a lifespan of about a year.[5]C. diadema has been observed to slough off in areas with high whale traffic, such as migration routes and breeding areas.[4][6]

Unlike coastal acorn barnacles which have been widely studied, the development of a whale barnacle was first researched in 2006 with Coronula diadema collected from the fin of a beached humpback whale. Immediately after hatching, the newly born nauplius larvae molted and, after six molts, reached the cyprid stage, the last stage before maturity. Unlike other barnacles, the stage II and III nauplius had a pair of horns projecting from the head, and the eyes in stage IV were crescent shaped. The cyprid had circular eyes and, like other barnacles, had several oil cells in the head which probably acted as food reserves as cyprids do not feed. The cyprids seemed to be induced to settle onto a substrate by a cue released from whale skin, though they do not have to settle on the skin. Though the mechanism is not fully understood, coastal barnacles receive settling cues from a certain protein, so it may be that whale barnacles use the alpha-2-macroglobulin, a plasma protein of the blood common in vertebrates. After settling, the juvenile barnacles formed a ring-shaped structure that firmly gripped onto the skin, growing upwards as a cylinder.[19] Wall plates did not form at first, though the juveniles did develop stripes. This cylindrical shape is similar to the adult T. major, which attaches to right whales.[19]

Cirri are used by barnacles to capture food particles in the current. The barnacles extend their cirri into a fan-shape, catch particles, and then retract the cirri back into the shell to transfer the particles into the mouth. First, a membrane—the opercular membrane shielding the barnacle from the water—is opened and the cirri emerge from the shell and are spread. At full extension, three of the six cirri do not protrude past the membrane. The cirri then do a forward stroke, and the long cirri and membrane begin retraction. They do a backward stroke and the cirri roll back up into the shell. In Cryptolepas, this process was observed as taking 1.2 to 1.9 seconds, however the forward and backward strokes can be skipped entirely, and the cirri can simply be extended and quickly coil back up. Adolescent barnacles have shorter cycles than adults. In fast currents, the cirri do not retract. Land-based barnacles have to reorient their cirri depending on the direction of the current; but since the current only flows in one direction for whale barnacles—from the head to the tail of the host—adults have lost that ability. However, the cirri do have a special function during copulation.[20] At this time, the barnacle acting as a male (barnacles are hermaphrodites) fully extends its cirri, and the penis begins a searching movement around its circumference. Having encountered another barnacle, the pair begin a series of intense cirral movements which was observed in Cryptolepas as lasting around 32 seconds.[20]

Whale barnacles typically attach to baleen whales and have a commensal relationship–the barnacle benefits and the whale is neither helped nor harmed.[3] A single humpback whale may carry up to 450 kg (990 lb) of barnacles.[21] Whale barnacles usually settle on patches of roughened, calcified skin called callosities. Infestations tend to form a unique pattern for an individual whale, and can be used as identifying markers by researchers and perhaps by other whales.[22] Since barnacles require that water flow independently over them to filter food, colonies may follow the direction of water currents produced by the animal in areas with moderate flow.[23] However, Xenobalanus exclusively inhabits the most turbulent environments for barnacles on flippers, flukes, and dorsal fins. Barnacle larvae may reach these sites passively, being deposited naturally by vortexes created by the animal, or may crawl to more suitable locations.[15]Xenobalanus stimulates the growth of calcified skin around itself which prevents the skin from shedding and dislodging the barnacle.[17] On baleen whales, barnacles are often found in conjuncture with whale lice.[23] The goose barnacle Conchoderma auritum often attaches to the shell of C. diadema.[14]

Though whale barnacles are generally considered to be commensals, callosities could be an adaptation to prevent barnacles from adding to drag by concentrating infestations,[22] and a heavy infestation may lead to eczema.[23]Xenobalanus can more easily grow on sick skin with a weakened immune system, and younger individuals tend to have larger infestations presumably because they are less resistant;[16] further, given it has a stalk, it increases the drag felt by the host and may be considered parasitic in that sense.[17] A Cryptolepas infection on beluga whales (Delphinapterus leucas) elicited an immune response by the skin, and the barnacles were ejected after a few weeks.[24] Gray whales have been observed rubbing against the gravelly seafloor to dislodge barnacles.[25]

Coronula on a gray whale

Conversely, some whales may use barnacles as weapons or protective armor to add power to a strike in mating battles or against killer whales (Orcinus orca), or as a deterrent to being bitten by killer whales. This would make the relationship between whale barnacles and certain whales mutualistic in which both parties benefit. It may be that some baleen whales, in the context of the fight-or-flight response, are adapted for a fight response, namely the humpback and gray (Eschricthius robustus) whales, and so evolved to attract barnacles, sacrificing speed for damage and defense; whereas others, the Balaenoptera, are adapted for a flight response, probably evolving an antifouling mechanism in their skin to deter infestations and avoiding unnecessary weight which would hinder speed. However, the bowhead whale (Balaena mysticetus) and the North Atlantic (Eubalaena glacialis) and North Pacific (E. japonica) right whales, which have fight responses, are generally barnacle-free,[21] though it may be that historic whaling, which reduced their populations, restricted their distribution and contact with other whales, thus impeding the barnacles' ability to infect other whales.[14]

C. diadema inhabits mainly the humpback whale (Megaptera novaengliae), but also the southern right whale (E. australis), the blue whale (Balaenoptera musculus), the fin whale (B. physalus), the sperm whale (Physeter macrocephalus), and the northern bottlenose whale (Hyperoodon ampullatus). C. reginae inhabits the humpback whale, blue whale, fin whale, sei whale (B. borealis), the common minke whale (B. acutorostrata), and the loggerhead sea turtle (Caretta caretta). Cetopirus inhabits exclusively the southern right whale. Cryptolepas almost exclusively inhabits the gray whale, but has been recorded on the killer whale, the beluga whale, and in the stomach of the topsmelt silverside (Atherinops affinis).[26] Topsmelt are known to pick off the dead skin and whale lice often found in association with barnacles.[25]T. major has been recorded on the southern right whale.[26][16]

^ abcdHayashi, R. (2012). "Atlas of the barnacles on marine vertebrates in Japanese waters including taxonomic review of superfamily Coronuloidea (Cirripedia: Thoracica)". Journal of the Marine Biological Association of the United Kingdom. 92 (1): 107–127. doi:10.1017/S0025315411000737.